Rapid protamine evolution suppresses meiotic drive in Drosophila

Many animal species replace histones with protamines during spermatogenesis. Although essential for sperm function, protamines evolve rapidly for reasons that remain unknown. Using in vivo gene replacement, we examined the causes and consequences of the rapid evolution of Mst77F, a protamine essential for male fertility in Drosophila melanogaster (D. melanogaster). Replacing Mst77F with divergent orthologs caused DNA compaction defects in X-bearing sperm, resulting in fewer mature X-bearing sperm and male-biased progeny. Reducing D. melanogaster Mst77F dosage caused the same bias, whereas increasing the dosage of Mst77F orthologs rescued it. Engineered sex chromosome fusions revealed that Mst77F protects the D. melanogaster X chromosome from a killer-target meiotic drive system in a dosage- and sequence-dependent manner. Unlike in D. melanogaster, Mst77F was dispensable for fertility in Drosophila yakuba (D. yakuba) but remained important for suppressing sex ratio distortion. Our findings show that relentless pressure to suppress sex chromosome meiotic drive underlies the rapid evolution of protamines.